Impact of preoperative biliary drainage on surgical risk in pancreaticoduodenectomy for resectable periampullary tumors

Introduction

Pancreaticoduodenectomy (PD), also known as the Whipple procedure, is a complex surgical technique used to treat various benign and malignant diseases affecting the pancreas, bile duct, and duodenum (1-3). It is the only potentially curative therapy for pancreatic and periampullary tumors, and one of the most specialized and challenging operations performed by gastrointestinal surgeons. However, since its first introduction in 1941, PD has been associated with high mortality rates. In recent years, with advancements in surgical techniques and postoperative care, the previously reported perioperative mortality rate of 20% to 30% has decreased to below 5% (4). The technical complexity of this procedure stems from the extensive scope of resection, the need for digestive tract reconstruction, the multiple anastomoses, the complex anatomy, and potential postoperative complications such as bile leakage, delayed gastric emptying and infection (5-8).

To alleviate jaundice, preoperative biliary stenting is commonly used in patients with benign or malignant biliary obstruction. This can relieve biliary obstruction, improve the patient’s general condition by enhancing hepatic synthetic function, increasing the clearance of endogenous toxins, and improving gastrointestinal mucosal function. However, the mechanical stimulation of the bile duct and the resulting local inflammatory response caused by biliary drainage may increase the difficulty of dissection and resection during surgery. Overall, the impact of preoperative biliary drainage (PBD) on intraoperative risk in Whipple surgery remains controversial. Based on the clinical data of patients who underwent PD in the General Surgery Center of Friendship Hospital, this study comprehensively considers factors such as whether PBD was performed and the method of biliary drainage to evaluate the difficulty of PD. We present this article in accordance with the TRIPOD reporting checklist (available at https://tgh.amegroups.com/article/view/10.21037/tgh-2025-161/rc).

Methods

Study subjects and surgical difficulty scoring method

A retrospective analysis was conducted on the clinical data of 354 patients with periampullary malignancies who underwent PD at Beijing Friendship Hospital, Capital Medical University, between June 2017 and October 2024. The cohort comprised 206 males and 148 females, with a median age of 62.5 (IQR, 58–67) years. The mean operative time was 305 minutes (range, 105–630 minutes), and the mean intraoperative blood loss was 425.88 mL (range, 50–3,500 mL). Among these patients, 113 underwent laparoscopic pancreaticoduodenectomy (LPD), including 41 conversions to open surgery, and 191 underwent open pancreaticoduodenectomy (OPD). As there is currently no universally accepted scoring system for assessing the surgical difficulty of laparoscopic and open PD, we referred to established scoring systems from high-quality clinical studies on laparoscopic liver and distal pancreatic surgery (6-8). In this study, the difficulty of PD was defined and scored as follows: one point was assigned for each of the following conditions—prolonged operative time, increased intraoperative blood loss, and open approach or conversion to open surgery; otherwise, zero points were assigned. The total score for each patient was obtained by summing the scores for operative time, intraoperative blood loss, and surgical approach, resulting in the following distribution: 0 points (n=27), 1 point (n=168), 2 points (n=135), and 3 points (n=24). Patients with total scores of 0–1 were classified as the low-difficulty group (n=195), and those with scores of 2–3 were classified as the high-difficulty group (n=159). The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Beijing Friendship Hospital, Capital Medical University (approval No. 2022-P2-104-01) and individual consent for this retrospective analysis was waived.

Inclusion and exclusion criteria

Inclusion criteria: (I) adults aged ≥18 years; (II) patients who underwent PD at Beijing Friendship Hospital, Capital Medical University, between June 2017 and October 2024.

Exclusion criteria: (I) concurrent cholangitis or pancreatitis upon admission; (II) prior biliary drainage before admission; (III) preoperative assessment indicating distant metastasis or borderline resectability requiring neoadjuvant therapy (NAT); (IV) coexistence of other primary malignant diseases; (V) severe organ dysfunction or serious comorbidities (e.g., severe cardiopulmonary or hepatic insufficiency) precluding surgery; (VI) pregnancy; (VII) refusal to participate in the study; (VIII) missing intraoperative data or missing more than 50% of other clinical data.

Data collection

Collected clinical data included patient sex, age, surgical approach, intraoperative blood loss, operative time, postoperative pathological type, perioperative hematological and biochemical parameters, PBD method, preoperative imaging findings, postoperative complications, and length of hospital stay.

PBD and PD methods

Preoperative biliary decompression methods included endoscopic nasobiliary drainage (ENBD), percutaneous transhepatic cholangial drainage (PTCD), and biliary stenting. All procedures were performed by experienced endoscopists from the Department of Gastroenterology at our center. All PDs were performed by senior attending surgeons with extensive experience, using either an open or laparoscopic approach. Standard regional lymph node dissection was performed in all cases. Digestive tract reconstruction was conducted using the Child method. PD was categorized as either mucosa-to-mucosa anastomosis or non-mucosa-to-mucosa anastomosis.

Statistical analysis

Data analyses were performed using SPSS version 26.0 and R version 4.2.1. Baseline data were expressed as categorical or continuous variables. For univariate comparisons between groups, continuous variables were tested for normality. Normally distributed data were analyzed using the independent-samples t-test (Mann-Whitney method), and non-normally distributed data were analyzed using the Mann-Whitney rank-sum test. Categorical variables were compared using the chi-squared test (asymptotic method only).

To construct a parsimonious model with optimal predictive performance, least absolute shrinkage and selection operator (LASSO) regression was applied. The optimal λ value was determined by 10-fold cross-validation, selecting the λ corresponding to the minimum mean error. Variables with nonzero coefficients at the optimal λ were included in the final model. Statistical analyses were performed using the glmnet package (version 4.1-8) in R 4.2.1. All multivariate analyses were conducted using binary logistic regression in SPSS 26.0.

Grouped dot plots for patients with PBD were visualized using the ggplot2 package in R. Multivariate forest plots for intraoperative blood loss, conversion to open surgery, and operative time in both the biliary drainage group and the overall cohort were generated using binary logistic regression in SPSS 26.0 and visualized with ggplot2 in R. All statistical tests were two-tailed, and a P value <0.05 was considered statistically significant.

Results

General data

A total of 354 patients were included in this study, comprising 195 patients in the low-difficulty group and 159 in the high-difficulty group. Regarding preoperative and postoperative indicators: Among the 354 enrolled patients, 184 did not undergo PBD, whereas 170 underwent PBD. Of those who underwent biliary drainage (Table 1). For patients who underwent biliary drainage, the duration from the biliary drainage procedure to the PD surgery was recorded as the biliary drainage period [median 13 days (IQR: 8–21 days)]. This study included a total of four chief complaint symptoms and six different types of postoperative pathological results (Figure 1). We grouped all patients who underwent PBD based on their drainage method and plotted the relevant clinical factors before and after drainage using grouped dot plots (Figure 2). Univariate analysis revealed that patients in the PTCD group had more severe preoperative biliary obstruction, as evidenced by higher levels of pre-drainage liver enzymes [alanine aminotransferase (ALT): 129 (IQR, 69–223) vs. 82 (IQR, 34–138) U/L] and higher bilirubin levels [total bilirubin (TB): 285 (IQR, 212–396) vs. 50 (IQR, 18–190) µmol/L]. Additionally, PTCD demonstrated efficacy in improving obstructive jaundice compared to endoscopic retrograde cholangiopancreatography (ERCP) [ΔTB: odds ratio (OR) =1.006, 95% confidence interval (CI): 1.003–1.009, P<0.001; ΔDB: OR =1.010, 95% CI: 1.005–1.015, P<0.001].

Figure 1 Clinical characteristics description of patients. (A) Doughnut chart of chief complaints at admission; (B) combined pie chart of case volume stratified by surgical difficulty; (C) doughnut chart of distribution of postoperative pathological findings; (D) histogram of duration of preoperative biliary drainage.

Figure 2 Changes in laboratory parameters following different biliary drainage procedures. (A) Scatter plot of WBC before and after preoperative biliary drainage; (B) scatter plot of TB before and after preoperative biliary drainage; (C) scatter plot of DB before and after preoperative biliary drainage direct bilirubin; (D) scatter plot of ALT before and after preoperative biliary drainage. ALT, alanine aminotransferase; DB, direct bilirubin; ERCP, endoscopic retrograde cholangiopancreatography; PTCD, percutaneous transhepatic cholangial drainage; TB, total bilirubin; WBC, white blood cell.

Factors influencing PD surgical complexity

In comparing the low-difficulty and high-difficulty groups, no significant differences were observed in patient gender, age, or pathological type grading and staging (all P>0.05). Preoperative clinical factors were analyzed using LASSO regression to identify significant predictors, resulting in the selection of six factors: PBD status, admission ALT, preoperative AST, preoperative CA125, preoperative hemoglobin (Hb), preoperative platelet count (PLT), and body mass index (BMI) (Figure 3). Logistic regression analysis indicated that PBD was an independent risk factor for increased surgical complexity (OR =1.615, 95% CI: 1.020–2.556, P=0.04) (Table 2). Further analysis of the impact of different biliary drainage methods on surgical complexity: Among the 170 patients who underwent PBD, various preoperative laboratory tests, imaging findings, chief complaints, symptom duration, clinical TNM staging, BMI, drainage method, and drainage duration were included in binary logistic regression. The results indicated that compared to retrograde drainage, antegrade drainage was associated with lower surgical complexity (OR =2.032, 95% CI: 1.016–4.064, P=0.045) (Table 3). Notably, regardless of whether considering all surgical patients (OR =1.130, 95% CI: 1.052–1.214, P<0.001) or only those undergoing biliary drainage (OR =1.110, 95% CI: 1.000–1.232, P<0.05), BMI was identified as an important factor contributing to increased surgical risk.

Figure 3 Identification of predictors for surgical risk using LASSO regression. (A) Cross-validation results for tuning parameter selection in the LASSO regression; (B) coefficient profile plot of the LASSO regression. LASSO, least absolute shrinkage and selection operator.

The impact of biliary drainage on components of surgical difficulty

To investigate how biliary drainage affects intraoperative bleeding, surgery duration, and surgical approach, we conducted univariate and multivariate binary logistic regression analyses with these factors as binary outcomes and plotted forest plots (Figure 4). The results indicated that for all PD patients, PBD and higher BMI were associated with increased risk of intraoperative bleeding (OR =1.603, 95% CI: 1.014–2.531, P<0.05) but did not significantly affect surgery duration or surgical approach. For patients who underwent PBD, those receiving ERCP drainage had a higher likelihood of conversion to open surgery (OR =2.370, 95% CI: 1.137–4.951, P<0.05) and greater intraoperative bleeding, although this did not reach statistical significance.

Figure 4 Risk factor analysis for components of surgical difficulty in all patients and in patients with preoperative biliary drainage. (A1) Forest plot of risk factors for intraoperative bleeding in patients with biliary drainage; (A2) forest plot of risk factors for intraoperative bleeding in all the patients; (B1) forest plot of risk factors for operative time in patients with biliary drainage; (B2) forest plot of risk factors for operative time in all the patients; (C1) forest plot of risk factors for conversion to laparotomy in patients with biliary drainage; (C2) forest plot of risk factors for conversion to laparotomy in all the patients. ALB, albumin; ALT, alanine aminotransferase; AST, aspartate aminotransferase; BMI, body mass index; CA125, carbohydrate antigen 125; CI, confidence interval; DB, direct bilirubin; ERCP, endoscopic retrograde cholangiopancreatography; Hb, hemoglobin; OR, odds ratio; PLT, platelet; PTCD, percutaneous transhepatic cholangial drainage; WBC, white blood cell.

Discussion

Malignant obstructive jaundice is a common clinical manifestation in patients with periampullary carcinoma. The state of obstructive jaundice can impair liver function, internal environment homeostasis, and immune function (9,10). For such patients, PBD is one of the most effective therapeutic measures for relieving obstructive jaundice. Current indications for PBD primarily include cholangitis, delayed surgery, and jaundice relief for patients scheduled to receive NAT; however, there remains no unified consensus on whether PBD should be routinely performed before PD (11,12). Some studies suggest that for patients planned for PD, PBD may increase the risk of abdominal and biliary infections, induce local inflammatory edema, and therefore recommend early surgery and avoidance of routine PBD (13-16). Conversely, other viewpoints indicate that PBD does not increase surgical risk or complications but rather helps improve the patient’s systemic condition and is beneficial for prognosis (17,18). Addressing this controversy, this single-center retrospective cohort study found that PBD is an independent risk factor for increased surgical risk in PD.

The main findings of this study are consistent with some research suggesting that PBD may increase surgical risk (19,20). The underlying mechanism may be that mechanical stimulation of the bile duct by biliary drainage devices (including stents or drainage tubes) can induce local inflammatory reactions and infection (21); such pathological changes may obscure the anatomical planes in the hepatic hilum, increasing the difficulty of dissection and consequently leading to increased intraoperative blood loss (19). Our subgroup analysis showed a significant correlation between PBD and increased intraoperative blood loss, supporting the above view. Furthermore, as described by Limongelli et al., PBD is prone to resulting in positive intraoperative bile bacterial cultures, which may exacerbate local inflammation and increase the risk of postoperative infectious complications (22), potentially explaining the increased surgical risk from another perspective.

Regarding the choice of drainage methods, PBD mainly includes two approaches: retrograde drainage via ERCP for stent placement or ENBD along the hepatopancreatic ampulla; and percutaneous transhepatic biliary drainage (PTBD), which involves percutaneous puncture and dilation of the bile duct for antegrade drainage (23). Due to its high clinical success rate, good patient convenience, and low complication rate, ERCP has become the preferred drainage method (24). In this study, regarding the impact of different drainage methods on PD surgical risk, we found that retrograde drainage (e.g., ERCP) was associated with higher surgical risk compared to antegrade drainage (e.g., PTBD). This result is partially consistent with the meta-analysis by Dorcaratto et al., which showed a lower complication rate for PTBD compared to ERCP in patients awaiting PD (25). Lermite et al. also reported a higher incidence of biliary infection after ERCP (26). However, the advantages and disadvantages of the two drainage methods remain debated. Some studies suggest that PTBD allows liver function to recover closer to normal levels preoperatively, facilitating surgery (27); while other studies support endoscopic stent placement being superior to percutaneous drainage (28). This study provides new evidence for this controversy from the perspective of surgical risk, suggesting that retrograde drainage, due to direct intervention in the ampulla and duodenal region, may cause more significant tissue edema and adhesion, thereby posing greater challenges during dissection and resection. This also explains the higher conversion-to-open rate in the ERCP group in this study.

Furthermore, this study also found differences in preoperative laboratory indicators among patients with different biliary drainage methods (Panel 2). The pre-drainage bilirubin level in the PTBD group was significantly higher than that in the ERCP group, and the post-drainage bilirubin decrease was greater in the PTBD group, suggesting that PTBD is more effective in relieving biliary obstruction.

Besides PBD, this study also confirmed that a higher BMI is a significant factor for increased surgical risk in PD, while serum albumin level showed no significant impact. This result echoes the research by Cui et al. on the impact of nutritional status on prognosis (29), suggesting that preoperative nutritional assessment and intervention may have positive significance for improving surgical outcomes in obese or overweight patients.

However, regarding the risks and value of biliary drainage, other studies have reached different conclusions. For instance, Sewnath et al. believed that PBD had no effect on postoperative complication rates (30); other studies showed that PBD did not affect the prognosis of PD patients (17,31). Furthermore, several studies reported that PBD was associated with a higher postoperative complication rate but found no association with intraoperative indicators such as blood loss and operation time (32). These discrepancies may stem from heterogeneity in study populations, drainage indications (routine drainage vs. selective drainage), the interval between drainage and surgery, and differences in surgeon experience. It is noteworthy that the traditional viewpoint supports preoperative drainage for patients with obstructive jaundice, especially those with severe liver function impairment or internal environment disturbances, believing that PBD can relieve cholestasis and improve the patient’s systemic condition for radical PD (33-35). This study does not entirely negate the value of PBD but emphasizes the need to carefully weigh its pros and cons. The key is to avoid a “one-size-fits-all” routine drainage strategy and adopt individualized selection: for patients with severe obstructive jaundice requiring delayed surgery, thorough preoperative preparation should be performed after biliary drainage; regarding the drainage method, PTBD may be an option with lower surgical risk if conditions permit.

This study has several limitations. First, the retrospective design inevitably introduces selection bias and confounding bias. Second, although the adopted surgical difficulty scoring system integrated surgical approach, time, and blood loss, and referenced the concept of difficulty scoring in laparoscopic liver and pancreatic surgery (36-38), it has not been repeatedly validated. Third, as a single-center study, the generalizability of its results requires further validation. Future research directions should include conducting prospective multicenter studies to validate this surgical difficulty scoring system and clarify the optimal indications for PBD. Meanwhile, prospective studies comparing the impact of different drainage strategies (e.g., ERCP vs. PTBD) on perioperative outcomes in comparable patient populations will also be highly valuable.

Conclusions

In summary, although PBD presents both benefits and harms for patients with malignant obstructive jaundice, concerning its impact on PD surgical difficulty, PBD is a risk factor. However, this does not mean we should completely reject the strategy of PBD. Rather, it necessitates more careful patient selection for PBD, avoiding indiscriminate preoperative drainage that could increase surgery-related risks for patients.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the TRIPOD reporting checklist. Available at https://tgh.amegroups.com/article/view/10.21037/tgh-2025-161/rc

Data Sharing Statement: Available at https://tgh.amegroups.com/article/view/10.21037/tgh-2025-161/dss

Peer Review File: Available at https://tgh.amegroups.com/article/view/10.21037/tgh-2025-161/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tgh.amegroups.com/article/view/10.21037/tgh-2025-161/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Beijing Friendship Hospital, Capital Medical University (approval No. 2022-P2-104-01) and individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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